K. M. Campbell A. F. Vaughn K. L. Russell B. Smith D. L. Jimenez C. P. Barrozo J. R. Minarcik N. F.Crum M. A. K. Ryan. Reportt No.
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1 NAVAL HEALTH RESEARCH CENTER RISK FACTORS FOR COMMUNITY-ACQUIRED METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS (CAMRSA) INFECTIONS IN MILITARY TRAINEES: REVIEW OF AN OUTBREAK IN SAN DIEGO, CALIFORNIA, 2002 K. M. Campbell A. F. Vaughn K. L. Russell B. Smith D. L. Jimenez C. P. Barrozo J. R. Minarcik N. F.Crum M. A. K. Ryan Reportt No Approved for public release; distribution unlimited. NAVAL HEALTH RESEARCH CENTER P. O. BOX SAN DIEGO, CA BUREAU OF MEDICINE AND SURGERY (M2) 2300 E ST. NW WASHINGTON, DC
2 Risk Factors for Community-Acquired Methicillin-Resistant Staphylococcus aureus (CAMRSA) Infections inmilitary Trainees: Review of an Outbreak in San Diego, California, 2002 Katherine M. Campbell 1 Andrew F. Vaughn, MD, MPH 2 Kevin L. Russell, MD, MTMH 1 Besa Smith 1 Dinice L. Jimenez 1 Christopher P. Barrozo 1 John R. Minarcik, MD 3 Nancy F.Crum, MD, MPH 3 Margaret A. K. Ryan, MD, MPH 1 1 Department of Defense Center for Deployment Health Research Naval Health Research Center P.O. Box San Diego, CA 2 Navy Environmental and Preventive Medicine Unit 5 San Diego, CA 3 Naval Medical Center San Diego San Diego, CA Corresponding author: Dr. Kevin Russell, Department of Defense Center for Deployment Health Research,, telephone (619) ; fax (619) ; Russell@nhrc.navy.mil Report No , was supported under work unit number TThe views expressed in this article are those of the authors and do not reflect the official policy or position of the Department of the Navy, Department of Defense, or the US Government. Approved for public release; distribution unlimited. This research has been conducted in compliance with all applicable federal regulations governing the protection of human subjects in research.
3 ABSTRACT An outbreak of community-acquired methicillin-resistant Staphylococcus aureus (CA- MRSA) skin infections was observed in a population of US military trainees in the summer of A questionnaire was developed and administered to 209 trainees, 22 of whom had MRSA 5 infections. Factors associated with infection were described by multivariable logistic regression modeling, and included having a roommate in training with a prior skin infection (odds ratio [OR] = 3.44), or having a family member or friend who worked in a healthcare setting (OR = 2.79). Previous antibiotic use, hospitalization, or health problems were not associated with MRSA infection. This outbreak of MRSA skin infections in an otherwise healthy, well-defined, 10 military population provided an opportunity to describe risk factors for CA-MRSA, which may help focus prevention efforts in this and other communities. 2
4 INTRODUCTION 15 Mounting evidence has confirmed that methicillin-resistant Staphylococcus aureus (MRSA), once based almost exclusively in healthcare facilities, is emerging as a communitybased pathogen. Recent reports indicate that the prevalence of community-acquired MRSA (CA- MRSA) infections is increasing (1, 4, 14, 17, 18, 22, 24), but even more concerning are the recent, numerous CA-MRSA outbreaks in groups of young, healthy individuals with no direct 20 ties to healthcare facilities and none of the typical risk factors for infection (6-10, 15, 16, 20, 23). Among the risk factors for CA-MRSA infection identified in previous investigations are prior antibiotic use, prior hospitalization, close contact with an MRSA-infected or colonized individual, injection drug use, and underlying illnesses (3, 5, 11, 25-27, 29). As CA-MRSA infections continue to become more widespread, additional investigation into the risk factors for 25 infection will be vital to the development and implementation of effective prevention and control measures. In this investigation, we examined potential risk factors for CA-MRSA infection in a population of military trainees. MATERIALS AND METHODS 30 Population. Young, healthy males who were enrolled in a 26-week, physically demanding military training program comprised the population for this investigation. During the course of the program, trainees lived and worked closely together and rarely left the training facility. As a result of this closed environment, trainees experienced relatively uniform exposures. Due to their frequent contact with sand, boats, equipment, and seawater during their training regimen, 35 trainees historically experienced a high occurrence of skin abrasions (Dr. Larry Garsha, US Navy, San Diego, Calif, September 2002, personal communication). 3
5 Outbreak identification. The first MRSA case was identified by the presence of cellulitis and a positive wound culture on August 2, Between August 2, 2002 and October 28, 2002 (12 40 weeks), a total of 34 MRSA infections were confirmed (figure 1). Four of those infections 45 occurred in trainees that had experienced a previous MRSA infection during this same 12-week period, and these were identified as repeat infections. The incidence of MRSA infection during this period was calculated as 9.5 cases per 1000 person-weeks. This was considered markedly higher than the baseline rate of cellulitis in this population, estimated at 3 cases per 1000 personweeks (Dr. Larry Garsha, US Navy, San Diego, September 2002, personal communication). Laboratory methods. Staphylococcal isolates from nasal swab specimens and wound cultures were sent to the Department of Defense Center for Deployment Health Research, San Diego, Calif, to provide additional molecular epidemiology for the outbreak. Clinical isolates were 50 examined for the presence of the meca gene, Panton-Valentine leukocidin (PVL) gene, and sequence type (ST) based on the method of multi-locus sequence typing (MLST) (12, 13, 19, 21). Outbreak intervention. During the course of the outbreak, several measures were implemented 55 in the trainee population to reduce the spread of infection. All trainees were required to apply mupirocin to their nares and to bathe with an antimicrobial skin cleanser on three separate occasions. In addition, the barracks were routinely disinfected with a 5% bleach solution. To identify any potential sources of MRSA carriage in this population, trainees and staff had their nares cultured several times. 4
6 60 Postoutbreak survey. As part of the outbreak investigation, a postoutbreak survey was developed to describe potential risk factors for CA-MRSA infection in this population. An optically scannable questionnaire was administered to 209 military trainees, representing approximately 70% of the available military trainee population, in October Data captured by the survey included demographic characteristics, medical characteristics, including prior antibiotic use, prior hospitalizations, medications, and allergies, and past medical history. Past medical history included questions about prior skin conditions. Trainees were also asked to provide information about dietary supplement use, tobacco and alcohol use, travel history, whether their roommate had been treated for a skin infection, whether 70 any members of their crew had been treated for a skin infection, whether they had a family member or friend who worked in a healthcare setting, and whether they had a family member who had recently been hospitalized or had an outpatient procedure. Self-reported data on prior hospitalizations, prior antibiotic use, and medication allergies were verified by medical records. 75 Statistical analyses. After descriptive investigation of population characteristics, analyses were performed to assess the significance of associations between the outcome (MRSA infection) and demographic and exposure variables. Using regression diagnostics, collinearity among variables was assessed. A manual backward stepwise logistic regression was conducted, with variables 80 considered for inclusion in the model if initial significance was characterized by p values < 0.15 from the univariate analysis. All covariates were investigated as possible confounders prior to removing them from further modeling. Multivariable logistic regression modeling was 5
7 performed; the reduced model included only those variables with significance characterized by p < 0.05 or otherwise identified as possible confounders. Results were reported as odds ratios 85 (ORs) and 95% confidence intervals (CIs) calculated for variables associated with MRSA infection. SAS software (Version 8.0, SAS Institute, Cary, NC) was used for analyses. RESULTS Based on testing of nasal swab specimens and wound cultures, military trainees were 90 classified as MRSA infected, MRSA colonized, or MRSA negative. Trainees who had a skin infection and tested positive for MRSA by wound culture of the infected area were classified as MRSA infected. Trainees who did not have a skin infection but whose nasal swab specimen tested positive for MRSA were classified as MRSA colonized. Trainees who did not have a skin infection and whose nasal swab specimen did not test positive for MRSA were classified as 95 MRSA negative. Of the 209 military trainees surveyed, 10.5% (n=22) were MRSA infected, 3.3% (n=7) were MRSA colonized, and 86.1% (n=180) were MRSA negative. Due to the small number, the 7 MRSA colonized cases were not included in further analyses. Questionnaire data for the remaining 202 trainees indicated that 77.2% were Caucasian, 67.4% were younger than 25 years old, 32.2% reported antibiotic use within the past 12 months, % reported a hospitalization within the past 24 months, 6.5% reported current dietary supplement use, 43.1% reported any tobacco use, and 46.5% reported current alcohol use (table 1). The variables identified through univariate analyses as being significantly associated with MRSA infection included antibiotic use within the 12 months prior to training (p=0.123), dietary 105 supplement use prior to training (p=0.110), having a roommate in training with a prior skin 6
8 infection (p=0.003), having a family member or friend who worked in a healthcare setting (p=0.013), and having a parent or member of the household who smoked during the trainee s childhood (p=0.007). Two variables were identified in the reduced logistic regression model as having a significant positive association with MRSA infection. Military trainees who reported 110 having a roommate in training with a prior skin infection had 3.4 times the odds of becoming infected with MRSA compared with trainees who did not report having a roommate with a skin infection (OR = 3.44; 95% CI, ). Trainees who reported having a family member or friend who worked in a healthcare setting had 2.8 times the odds of becoming infected with MRSA compared with trainees who did not report such ties to the healthcare field (OR = 2.79; % CI, ) (table 1). Conversely, having a parent or other household member who smoked during the trainee s childhood was negatively associated with MRSA infection; trainees who reported this appeared less likely to develop an MRSA infection compared with those who did not report such environmental tobacco exposure (OR = 0.26; 95% CI, ). 120 Laboratory results. Staphylococcal isolates from all 22 MRSA-infected individuals tested positive for the meca and PVL genes. In addition, all 22 isolates were identified as ST8 by MLST. DISCUSSION 125 The steady increase in reports of CA-MRSA outbreaks in young, healthy populations with no apparent risk factors for infection is concerning. With each outbreak, it is important to determine the possible risk factors for infection in order to focus prevention and control efforts. 7
9 This outbreak of CA-MRSA occurred in a young, healthy, and well-defined population of military trainees. During the course of their 26-week intense training regimen, these trainees 130 lived and worked closely together. In this environment, a small number of initial MRSA cases quickly became noticed as an outbreak. The control measures implemented within this military trainee population during the summer and fall of 2002 were apparently effective in stopping the MRSA outbreak. During its 12-week course, however, the affected population incurred a high cost from infections. At least trainees were hospitalized due to their MRSA infection, and 8 trainees were unable to complete their original training program, and therefore had to restart. Although these hospitalization and lost-time rates were higher than would be expected for a healthy trainee population, the voluntary drop rate for this trainee population was actually much lower than expected. Only 1 trainee reported dropping the training program after his MRSA infection. 140 In this outbreak investigation, the major risk factor associated with MRSA infection was having a roommate during training with a prior skin infection. This finding is consistent with data from previous studies that identify close contact with an MRSA-infected or colonized individual as a risk factor for infection (11, 27). Another risk factor associated with MRSA infection in this outbreak was having a family member or friend who worked in a healthcare 145 setting. This finding suggests that this CA-MRSA outbreak may have had indirect ties to healthcare facilities from trainees past contact with family and friends, a factor that has also been suggested in previous studies of MRSA infection (25). Finally, these statistical analyses identified having a parent or other household member who smoked during the trainee s childhood as protective against MRSA infection. Although difficult to explain, one might 150 speculate that childhood environmental tobacco smoke exposure is a surrogate for other 8
10 factor(s), perhaps immunologic, that are protective against infection. Note than none of these trainees had asthma or reactive airway disease; therefore, those exposed to environmental smoke as children may represent a subgroup with especially strong immune profiles (2). It is important to note that other factors, that have been associated with CA-MRSA 155 infection in previous studies of CA-MRSA infection, including past antibiotic use and prior hospitalization, were not found to be associated with MRSA infection in this present investigation. This implies that this population of otherwise healthy, strong, young adults may be different from other populations affected by MRSA. The results of the laboratory testing of staphylococcal isolates conducted in this outbreak 160 investigation are consistent with those of other CA-MRSA outbreaks. The presence of the meca gene in the 22 isolates is consistent with the finding of methicillin-resistance among these pathogens (21). In addition, the PVL gene is a potential virulence factor that has been linked to other CA-MRSA infections (19, 28). Finally, the identification of all 22 MRSA isolates as ST8 by MLST indicates that a single MRSA clone was present in this outbreak. Community- and 165 hospital-acquired MRSA outbreaks with ST8 have been identified previously within the United States (28). The limitations of this study include the small sample size and the unique population. As a result, the findings of this investigation may not be generalizable. There are inherent limitations to the use of survey data, including recall and response biases. It may be notable that the 70% 170 response rate is strong and some survey data were confirmed via medical record review. Despite limitations, this outbreak investigation included strengths that may contribute to our expanding understanding of CA-MRSA infections. Most notably, the outbreak occurred in a well-defined population of young, healthy, military trainees who experienced relatively uniform 9
11 exposures in their environment. In this controlled setting, one may have more confidence that 175 factors found to be associated with infection are true risk factors. The control measures implemented during this outbreak may have helped reduce the transmission of MRSA between trainees who had close contact but were not roommates, such as trainees who were members of the same crew. However, the data suggest that control measures did not eliminate the risk of MRSA transmission between roommates. Targeting education, 180 hygiene, and personal behaviors may be key to reducing the spread of MRSA among those with close physical contact in future outbreaks. Future studies may also explore the immunologic mechanisms that appear to make some otherwise healthy adults at higher risk for MRSA infections. 10
12 ACKNOWLEDGMENTS We appreciate the contributions and support of Dr. Brad Hale from Naval Medical Center, San Diego; Dr. Larry Garsha, Dr. Paul Ware, and Chief Jennifer Segarra from Naval Special Warfare Center, San Diego; Dr. Scott Sherman and Dr. Dennis Faix from Navy Environmental and Preventive Medicine Unit 5, San Diego; Col Dana Bradshaw and Col Gary Gackstetter from Uniformed Services University of Health Sciences, Bethesda, MD; and Ms. Lesley Henry and Ms. Rosha Aran from Naval Health Research Center, San Diego.
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15 16. Herold, B. C., L. C. Immergluck, M. C. Maranan, D. S. Lauderdale, R. E. Gaskin, S. Boyle-Vavra, C. D. Leitch, and R. S. Daum Community-acquired methicillinresistant Staphylococcus aureus in children with no identified predisposing risk. JAMA 279: Kallen, A. J., T. J. Driscoll, S. Thornton, P. E. Olson, and M. R. Wallace Increase in community-acquired methicillin-resistant Staphylococcus aureus at a Naval Medical Center. Infect Control Hosp Epidemiol 21: Layton, M. C., W. J. Hierholzer, Jr., and J. E. Patterson The evolving epidemiology of methicillin-resistant Staphylococcus aureus at a university hospital. Infect Control Hosp Epidemiol 16: Lina, G., Y. Piémont, F. Godail-Gamot, M. Bes, M. O. Peter, V. Gauduchon, F. Vandenesch, and J. Etienne Involvement of Panton-Valentine leukocidinproducing Staphylococcus aureus in primary skin infections and pneumonia. Clin Infect Dis 29: Lindenmayer, J. M., S. Schoenfeld, R. O'Grady, and J. K. Carney Methicillinresistant Staphylococcus aureus in a high school wrestling team and the surrounding community. Arch Intern Med 158: Louie, L., S. O. Matsumura, E. Choi, M. Louie, and A. E. Simor Evaluation of three rapid methods for detection of methicillin resistance in Staphylococcus aureus. J Clin Microbiol 38: Moreno, F., C. Crisp, J. H. Jorgensen, and J. E. Patterson Methicillin-resistant Staphylococcus aureus as a community organism. Clin Infect Dis 21:
16 23. Pan, E. S., B. A. Diep, H. A. Carleton, E. D. Charlebois, G. F. Sensabaugh, B. L. Haller, and F. Perdreau-Remington Increasing prevalence of methicillinresistant Staphylococcus aureus infection in California jails. Clin Infect Dis 37: Saiman, L., M. O'Keefe, P. L. Graham, 3rd, F. Wu, B. Saïd-Salim, B. Kreiswirth, A. LaSala, P. M. Schlievert, and P. Della-Latta Hospital transmission of community-acquired methicillin-resistant Staphylococcus aureus among postpartum women. Clin Infect Dis 37: Salgado, C. D., B. M. Farr, and D. P. Calfee Community-acquired methicillinresistant Staphylococcus aureus: a meta-analysis of prevalence and risk factors. Clin Infect Dis 36: Saravolatz, L. D., N. Markowitz, L. Arking, D. Pohlod, and E. Fisher Methicillin-resistant Staphylococcus aureus. Epidemiologic observations during a community-acquired outbreak. Ann Intern Med 96: Saravolatz, L. D., D. J. Pohlod, and L. M. Arking Community-acquired methicillin-resistant Staphylococcus aureus infections: a new source for nosocomial outbreaks. Ann Intern Med 97: Vandenesch, F., T. Naimi, M. C. Enright, G. Lina, G. R. Nimmo, H. Heffernan, N. Liassine, M. Bes, T. Greenland, M. E. Reverdy, and J. Etienne Communityacquired methicillin-resistant Staphylococcus aureus carrying Panton-Valentine leukocidin genes: worldwide emergence. Emerg Infect Dis 9: Warshawsky, B., Z. Hussain, D. B. Gregson, R. Alder, M. Austin, D. Bruckschwaiger, A. H. Chagla, J. Daley, C. Duhaime, K. McGhie, G. Pollett, H. Potters, and L. Schiedel Hospital- and community-based surveillance of 15
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18 Table 1. Characteristics of survey responders and associations with MRSA infection Variable Total N MRSA infected OR * CI * Number % Number % Race/ethnicity NSS Caucasian Other Age (y) NSS < > Antibiotic use within past 12 months NSS Hospitalization within past NSS 24 months Currently taking a dietary NSS supplement Any past or current NSS tobacco use Current alcohol use NSS Having a roommate during training with a prior skin infection Having a family member or friend who worked in a healthcare setting Having a parent or member of the household who smoked during the respondent s childhood , , , 0.94 * Adjusted odds ratio (OR) and 95% confidence interval (CI) based on multivariable logistic regression modeling. NSS = not statistically significant. 17
19 Legend for figure Figure 1. Number of MRSA cases in the military trainee population during each week of the 2002 outbreak. 18
20 Figure Cases Aug 9-Aug 16-Aug 23-Aug 30-Aug 6-Sep 13-Sep 20-Sep 27-Sep 4-Oct 11-Oct 18-Oct 25-Oct Week
21 REPORT DOCUMENTATION PAGE The public reporting burden for this collection of information is estimated to average 1 hour per response, including the time for reviewing instructions, searching existing data sources, gathering and maintaining the data needed, and completing and reviewing the collection of information. Send comments regarding this burden estimate or any other aspect of this collection of information, including suggestions for reducing the burden, to Washington Headquarters Services, Directorate for Information Operations and Reports, 1215 Jefferson Davis Highway, Suite 1204, Arlington, VA , Respondents should be aware that notwithstanding any other provision of law, no person shall be subject to any penalty for failing to comply with a collection of information if it does not display a currently valid OMB Control number. PLEASE DO NOT RETURN YOUR FORM TO THE ABOVE ADDRESS. 1. Report Date (DD MM YY) Report Type New 4. TITLE AND SUBTITLE Risk Factors for Community-Acquired Methicillin-Resistant Staphylococcus aureus (CA-MRSA) Infections in Military Trainees: Review of an Outbreak in San Diego, California, AUTHORS Katherine M. Campbell, Andrew F. Vaughn, Kevin L. Russell, Besa Smith, Dinice L. Jimenez, Christopher P. Barrozo, John R. Minarcik, Nancy F. Crum, Margaret A. K. Ryan 7. PERFORMING ORGANIZATION NAME(S) AND ADDRESS(ES) Naval Health Research Center P.O. Box San Diego, CA SPONSORING/MONITORING AGENCY NAMES(S) AND ADDRESS(ES) Chief, Bureau of Medicine and Surgery Code M E St NW Washington DC DATES COVERED (from - to) August 2002 October a. Contract Number: 5b. Grant Number: 5c. Program Element: 5d. Project Number: 5e. Task Number: 5f. Work Unit Number: g. IRB Protocol Number: PERFORMING ORGANIZATION REPORT NUMBER Report No Sponsor/Monitor's Acronyms(s) 11. Sponsor/Monitor's Report Number(s) 12 DISTRIBUTION/AVAILABILITY STATEMENT Approved for public release; distribution unlimited. 13. SUPPLEMENTARY NOTES Published in J Clin Microbiol Sep;42(9): ABSTRACT (maximum 200 words) An outbreak of community-acquired methicillin-resistant Staphylococcus aureus (CA-MRSA) skin infections was observed in a population of US military trainees in the summer of A questionnaire was developed and administered to 209 trainees, 22 of whom had MRSA infections. Factors associated with infection were described by multivariable logistic regression modeling, and included having a roommate in training with a prior skin infection (odds ratio [OR] = 3.44), or having a family member or friend who worked in a healthcare setting (OR = 2.79). Previous antibiotic use, hospitalization, or health problems were not associated with MRSA infection. This outbreak of MRSA skin infections in an otherwise healthy, well-defined, military population provided an opportunity to describe risk factors for CA-MRSA, which may help focus prevention efforts in this and other communities. 15. SUBJECT TERMS methicillin-resistant Staphylococcus aureus, military trainees, public health, outbreak investigation, CA-MRSA 16. SECURITY CLASSIFICATION OF: 17. LIMITATION 18. NUMBER 19a. NAME OF RESPONSIBLE PERSON a. REPORT b.abstract c. THIS PAGE OF ABSTRACT OF PAGES Commanding Officer UNCL UNCL UNCL UNCL 19b. TELEPHONE NUMBER (INCLUDING AREA CODE) COMM/DSN: (619) Standard Form 298 (Rev. 8-98) Prescribed by ANSI Std. Z39-18
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